Plant immunity triggered by engineered in vivo release of oligogalacturonides, damage-associated molecular patterns

• Published in: Proceedings of the National Academy of Sciences - PNAS 2015-04, Vol.112 (17), p.5533-5538
• Main Authors: Benedetti, Manuel, Pontiggia, Daniela, Raggi, Sara, Cheng, Zhenyu, Scaloni, Flavio, Ferrari, Simone, Ausubel, Frederick M., Cervone, Felice, DeLorenzo, Giulia
• Format: Article
• Language: English
• Subjects: Animals; Arabidopsis; Arabidopsis - genetics; Arabidopsis - immunology; Arabidopsis - metabolism; Arabidopsis - microbiology; Arabidopsis Proteins - biosynthesis; Arabidopsis Proteins - genetics; Arabidopsis Proteins - immunology; Biological Sciences; Botrytis - growth & development; Botrytis - immunology; Botrytis cinerea; Enzymes; Flowers & plants; Fungal Proteins - biosynthesis; Fungal Proteins - genetics; Fungal Proteins - immunology; Hexuronic Acids - immunology; Hexuronic Acids - metabolism; Immune system; Mice, Transgenic; Molecules; Pathogens; Pectin; Pectobacterium; Pectobacterium carotovorum - growth & development; Pectobacterium carotovorum - immunology; Plant Diseases - genetics; Plant Diseases - immunology; Plant Diseases - microbiology; Plant Immunity; Plant Proteins - biosynthesis; Plant Proteins - genetics; Plant Proteins - immunology; Polygalacturonase - biosynthesis; Polygalacturonase - genetics; Polygalacturonase - immunology; Pseudomonas syringae; Pseudomonas syringae - growth & development; Pseudomonas syringae - immunology; Recombinant Fusion Proteins - biosynthesis; Recombinant Fusion Proteins - genetics; Recombinant Fusion Proteins - immunology; Transgenic plants
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1504154112

Significance Damage-associated molecular patterns (DAMPs), released from host tissues as a consequence of pathogen attack, have been proposed as endogenous activators of immune responses in both animals and plants. Oligogalacturonides (OGs), oligomers of α-1,4–linked galacturonic acid generated in vitro by the partial hydrolysis of pectin, have been shown to function as potent elicitors of immunity when they are applied exogenously to plant tissues. However, there is no direct evidence that OGs can be produced in vivo or that they function as immune elicitors. This report provides the missing evidence that OGs can be generated in planta and can function as DAMPs in the activation of plant immunity. Oligogalacturonides (OGs) are fragments of pectin that activate plant innate immunity by functioning as damage-associated molecular patterns (DAMPs). We set out to test the hypothesis that OGs are generated in planta by partial inhibition of pathogen-encoded polygalacturonases (PGs). A gene encoding a fungal PG was fused with a gene encoding a plant polygalacturonase-inhibiting protein (PGIP) and expressed in transgenic Arabidopsis plants. We show that expression of the PGIP–PG chimera results in the in vivo production of OGs that can be detected by mass spectrometric analysis. Transgenic plants expressing the chimera under control of a pathogen-inducible promoter are more resistant to the phytopathogens Botrytis cinerea , Pectobacterium carotovorum , and Pseudomonas syringae . These data provide strong evidence for the hypothesis that OGs released in vivo act as a DAMP signal to trigger plant immunity and suggest that controlled release of these molecules upon infection may be a valuable tool to protect plants against infectious diseases. On the other hand, elevated levels of expression of the chimera cause the accumulation of salicylic acid, reduced growth, and eventually lead to plant death, consistent with the current notion that trade-off occurs between growth and defense.